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Melo-Ferreira J, Lemos De Matos A, Areal H, Lissovski A, Carneiro M, Esteves PJ (2015) The

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Melo-Ferreira J, Lemos De Matos A, Areal H, Lissovski A, Carneiro M, Esteves PJ (2015) The 1 This is the Accepted version of the following article: 2 Melo-Ferreira J, Lemos de Matos A, Areal H, Lissovski A, Carneiro M, Esteves PJ (2015) The 3 phylogeny of pikas (Ochotona) inferred from a multilocus coalescent approach. Molecular 4 Phylogenetics and Evolution 84, 240-244. 5 The original publication can be found here: 6 https://www.sciencedirect.com/science/article/pii/S1055790315000081 7 8 The phylogeny of pikas (Ochotona) inferred from a multilocus coalescent approach 9 10 José Melo-Ferreiraa,*, Ana Lemos de Matosa,b, Helena Areala,b, Andrey A. Lissovskyc, Miguel 11 Carneiroa, Pedro J. Estevesa,d 12 13 aCIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, 14 InBIO, Laboratório Associado, Campus Agrário de Vairão, 4485-661 Vairão, Portugal 15 bDepartamento de Biologia, Faculdade de Ciências, Universidade do Porto, 4099-002 Porto, 16 Portugal 17 cZoological Museum of Moscow State University, B. Nikitskaya, 6, Moscow 125009, Russia 18 dCITS, Centro de Investigação em Tecnologias da Saúde, IPSN, CESPU, Gandra, Portugal 19 20 *Corresponding author: José Melo-Ferreira. CIBIO, Centro de Investigação em Biodiversidade e provided by Repositório Aberto da Universidade do Porto View metadata, citation and similar papers at core.ac.uk CORE brought to you by 21 Recursos Genéticos, Universidade do Porto, InBIO Laboratório Associado, Campus Agrário de 22 Vairão, 4485-661 Vairão. Phone: +351 252660411. E-mail: [email protected]. 23 1 1 Abstract 2 3 The clarification of the systematics of pikas (genus Ochotona) has been hindered by largely 4 overlapping morphological characters among species and the lack of a comprehensive molecular 5 phylogeny. Here we estimate the first multilocus phylogeny of the genus to date, by analysing 12 6 nuclear DNA markers (total of 7.5 Kb) in 11 species of pikas from the four classified subgenera 7 (Pika, Ochotona, Lagotona and Conothoa) using a multispecies coalescent-based framework. The 8 species-tree confirmed the subgeneric classification by retrieving as monophyletic the subgenera 9 represented here by more than one species. Contrary to previous phylogenies based on mtDNA 10 alone, Lagotona was found to be sister to Pika. Also, support for the monophyly of the alpina group 11 was not strong, thus caution should be used in future analyses of this group. A relaxed molecular 12 clock calibrated using the Ochotonidae-Leporidae divergence resulted in more recent estimates of 13 divergence times relative to previous studies. Strong concordance with inferences based on fossil 14 records was found, suggesting that the initial diversification of the genus took place by the end of 15 late Miocene. Finally, this work sets up methodologies and gathers molecular markers that can be 16 used to extend the understanding of the evolutionary history of the genus. 17 18 Keywords: Multilocus Coalescent; Ochotona; Pika; Relaxed Molecular Clock; Species-tree; 19 Systematics. 20 21 1. Introduction 22 23 Methods that allow reconstructing the phylogeny of species in a multilocus perspective, taking into 24 account the coalescence of different loci, provide a good opportunity to clarify the systematics of 25 taxonomic groups with traditionally confusing classifications and evolutionary histories. This 2 1 remains true in cases where phylogenies based on the widely used mitochondrial DNA are the sole 2 source of phylogenetic information available at the molecular level, because single-gene 3 phylogenies can often result in erroneous representations of the true species-tree given the variance 4 associated to the evolutionary process among loci (Maddison, 1997). Pikas (family Ochotonidae) 5 are one of such groups. 6 7 Pikas comprise a single extant genus, Ochotona Link, 1795, and with rabbits and hares (family 8 Leporidae) form the order Lagomorpha. Pikas are endemic to the Holarctic Region and the 28 9 recognized living species of pikas are currently mostly restricted to Asia (26 species), with the 10 remaining species inhabiting North America (Lissovsky, 2014). However, pikas are known to have 11 had a more extensive distribution range throughout the Pleistocene. For example, even though the 12 steppe pika (O. pusilla) is today restricted to the central Russian steppes and northern Kazakhstan, 13 fossil records show that during the Pleistocene its range extended to Western Europe (see e.g. 14 Erbajeva and Zheng, 2005 and references therein). 15 16 The attempts to establish a robust phylogeny of pikas have been complicated by the largely 17 overlapping morphological characteristics of extant and fossil species (see Erbajeva and Zheng, 18 2005; Hoffmann and Smith, 2005) and by the use of limited molecular phylogenetic approaches. 19 Phylogenetic relationships in this group were to date inferred solely based on mitochondrial DNA 20 (Yu et al., 2000; Niu et al., 2004; Lanier and Olson, 2009; Ge et al., 2013; Lissovsky, 2014). Some 21 hypotheses have nevertheless resulted from these studies. For example, Yu et al. (2000) suggested 22 that three major evolutionary groups may exist in Ochotona, a northern subgroup, a shrub–steppe 23 dwelling subgroup, and a mountain subgroup, which motivated the partition of species among three 24 subgenera, Pika, Conothoa, and Ochotona, respectively (Hoffmann and Smith, 2005). Later 25 mtDNA phylogenies using a more representative sampling of species suggested some 3 1 rearrangements of taxa among subgenera (Lanier and Olson, 2009; Lissovsky, 2014) or even the 2 inclusion of a fourth subgenus, Lagotona, comprising only O. pusilla (Lissovsky, 2014). However, 3 robust inferences of the relationships among species still await more powerful multilocus analyses. 4 5 Here the first multilocus phylogeny to date – 12 nuclear loci for a total of 7.5 kb – was inferred for 6 11 pika species applying a coalescent-based phylogeny reconstruction method. 7 8 2. Materials and methods 9 10 2.1. Sampling and laboratory work 11 12 A total of 11 pika species, about a third of all presently described Ochotona species, and 12 13 molecular markers were combined in this study. The four subgenera according to Lissovsky (2014), 14 Conothoa, Ochotona, Pika, and Lagotona, were represented in the sampling (Table 1; Fig. 1; see 15 ranges of the sampled species in Smith et al., 1990, Lissovsky et al., 2007 and Smith and Xie, 16 2008), and at least two individuals per species were newly sequenced for each marker. The only 17 exception was O. princeps with one newly sequenced individual to which sequences available in 18 GenBank and Ensembl were added to represent a second specimen (see Suppl. Table 1 for 19 accession numbers). Of the analyzed markers, nine were autosomal (ALB, DARC, OXA1L, PPOX, 20 PRKCI, SPTBN1, TSHB, UCP2 and UCP4; Matthee et al., 2004; Alves et al., 2008; Melo-Ferreira 21 et al., 2009; Melo-Ferreira et al., 2012) and three were X-linked (AMOT, GRIA3 and IL1RAPL1; 22 Carneiro et al., 2010) (see Suppl. Table 2). 23 24 Total genomic DNA was extracted from liver, muscle or testis tissues using the E.Z.N.A. Tissue 25 DNA Kit (Omega Bio-Tek, Norcross, GA, USA) according to manufactures’ instructions. The 12 4 1 loci were PCR amplified using the primers indicated in Suppl. Table 2. Sequencing was performed 2 in both directions with an ABI PRISM 3130 Genetic Analyser (Applied Biosystems, Foster City), 3 following the ABI PRISM BigDye Terminator Cycle sequencing protocol. 4 5 2.2. Data Analyses 6 7 The nucleotide sequences were edited using BioEdit (Hall, 1999) and aligned with ClustalW 8 (Thompson et al., 1994). Haplotypes were reconstructed for each individual using PHASE v2.1 9 (Stephens and Donnelly, 2003), implemented in DnaSP v5.10.01 (Librado and Rozas, 2009). The 10 best-fit of several substitution models to each locus was assessed using jModeltest (Posada, 2008) 11 and the Akaike information criterion (AIC). Given that the phylogenetic method to be used (see 12 below) assumes no intra-locus recombination, a second dataset was produced using IMgc (Woerner 13 et al., 2007), retaining the largest non-recombining blocks per locus. A balance between the number 14 of sequences and length was looked for in order to keep at least one sequence per species per locus 15 in the recombination-free data set. 16 17 Sequences from Lepus granatensis were included in the dataset as outgroup. For the X-linked loci, 18 sequences were retrieved from Carneiro et al. (2010) and one additional specimen was newly 19 sequenced for all loci. For the remaining loci, sequences from specimens Lgr2 and Lgr7 from Melo- 20 Ferreira et al. (2012) were used. 21 22 Phylogenetic reconstruction was performed using the multilocus species-tree coalescent-based 23 method implemented in *BEAST v1.8.0 (Drummond et al., 2012) both for the complete and 24 recombination-free alignments. The Yule process and an uncorrelated lognormal relaxed clock 25 model were used. The mutation model was set based on the AIC results of jModeltest, or if the 5 1 specific model was not implemented in *BEAST, the next most parameterized model was selected. 2 Three independent runs of 100 000 000 generations with low autocorrelation of the Markov chain 3 Monte Carlo (MCMC) chain, as examined using Tracer v1.5 (Rambaut and Drummond, 2007), 4 were concatenated using LogCombiner, discarding the first 10% as burn-in. Trees were then 5 summarized with TreeAnnotator, also part of the BEAST package. FigTree v1.3.1 6 (http://tree.bio.ed.ac.uk/software/figtree/) was used to display the inferred species-tree. 7 8 Similarly to the strategy used by Lanier and Olson (2009), calibration of the species-tree was 9 performed considering three possible dates of divergence between Ochotonidae and Leporidae to 10 scale the root mean height: 31 Mya (Matthee et al., 2004), 37 Mya (McKenna and Bell, 1997; Asher 11 et al., 2005) and 65 Mya (Bininda-Emonds et al., 2007).
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